Response Linearity of Alert Monkey Non-Eye Movement Vestibular Nucleus Neurons During Sinusoidal Yaw Rotation

Abstract

Newlands SD, Lin N, Wei M. Response linearity of alert monkey non-eye movement vestibular nucleus neurons during sinusoidal yaw rotation. J Neurophysiol 102: 1388 -1397, 2009. First published June 24, 2009 doi:10.1152/jn.90914.2008. Vestibular afferents display linear responses over a range of amplitudes and frequencies, but comparable data for central vestibular neurons are lacking. To examine the effect of stimulus frequency and magnitude on the response sensitivity and linearity of non-eye movement central vestibular neurons, we recorded from the vestibular nuclei in awake rhesus macaques during sinusoidal yaw rotation at frequencies between 0.1 and 2 Hz and between 7.5 and 210°/s peak velocity. The dynamics of the neurons' responses across frequencies, while holding peak velocity constant, was consistent with previous studies. However, as the peak velocity was varied, while holding the frequency constant, neurons demonstrated lower sensitivities with increasing peak velocity, even at the lowest peak velocities tested. With increasing peak velocity, the proportion of neurons that silenced during a portion of the response increased. However, the decrease in sensitivity of these neurons with higher peak velocities of rotation was not due to increased silencing during the inhibitory portion of the cycle. Rather the neurons displayed peak firing rates that did not increase in proportion to head velocity as the peak velocity of rotation increased. These data suggest that, unlike vestibular afferents, the central vestibular neurons without eye movement sensitivity examined in this study do not follow linear systems principles even at low velocities. I N T R O D U C T I O NResponses of mammalian vestibular neurons, both peripheral and central, have been described for various stimulation paradigms. In vestibular afferent fibers, trade-off between the sensitivity of the cell's response and its linear range has been reported. Slow firing but sensitive irregular afferents effectively code acceleration only in the excitatory direction because once the firing rate of the neuron reaches inhibitory cutoff (rate of zero) the response of the cell remains zero (unchanged) with progressively more vigorous stimulation (Goldberg and Fernandez 1971b). Although the dynamics of vestibular afferent responses have been discussed extensively, less well understood is the impact of inhibitory cutoff and other nonlinearities in central vestibular neurons on the function of the vestibular system overall. Despite the known asymmetries in the primary afferent discharge, central mechanisms, especially the presence of a commissural system that provides informational redundancy in the vestibular nuclei, have been proposed to fill in the missing inhibitory information from one side of the midline with excitatory information from the other side (Abend 1978) to enable a linear output. Other authors have speculated on the possibilities of nonlinear processing in the central vestibular system ) and the role of population coding, which might provide...

Sensory convergence in the parieto-insular vestibular cortex

“…One female and one male rhesus macaque (Macaca mulatta), each weighing ϳ4 kg, were used in these experiments. The details of the surgical implantation of the head restraint, recording chamber, and eye coils have been previously published (Newlands et al 2009). Initially, a head-restraint post was implanted in dental acrylic that was attached to the monkey's skull via surgically implanted, transcranial stainless steel T-bolts.…”

“…Many elements of the data analysis have been described elsewhere (Newlands et al 2009). In brief, the recorded neural signal was triggered offline using a combination of timeamplitude windows and spike-waveform-principle components to create a spike time stamp.…”

“…Because many PIVC cells are slow firing, we used a Kaiser window filter (cutoff frequency 0.4 Hz, bandpass 5.0 Hz) to convert the time stamp from the spikes into a continuous function (Cherif et al 2008), which was then compared with the digitized stimuli (eye position, head position, and chair-rotator position) to calculate the response sensitivity or gain (the peak-to-peak output of the neuron/peak-to-peak stimulus in spikes per second per degree per second) and phase (the relative timing of the peak of the response to the peak of the stimulus). Accurate fitting of the neural responses that rectified during rotation in one direction required that sensitivity and phase were computed using a nonlinear least-squares algorithm (Levenberg-Marquardt method, see Newlands et al 2009). Gains were computed relative to horizontal head velocity during whole-body and head-on-neck rotations and to chair rotational velocity during trunk-only rotations.…”

Improving spatial updating accuracy in absence of external feedback

“…In addition, because the same neural networks process vestibular information (Newlands et al, 2009), regardless of body rotation direction, calibrating vestibular perception could transfer to the untrained direction. In that regard, small but significant reduction of the spatial error was observed when transferred in the untrained direction, regardless of the presence of external feedback or not during practice.…”

Mechanisms of Sustained High Firing Rates in Two Classes of Vestibular Nucleus Neurons: Differential Contributions of Resurgent Na, Kv3, and BK Currents

“…Mammalian vestibular nucleus neurons, for example, fire spontaneously in the awake animal at baseline firing rates of about 30 -100 Hz and can increase firing rates up to several hundred Hz (Beraneck and Cullen 2007;Buettner et al 1978;Cheron et al 1996;Cullen and McCrea 1993;Fuchs and Kimm 1975;Newlands et al 2009;Ris et al1995). To sustain high firing rates, neurons must overcome a critical challenge presented by the biophysical properties of sodium channels: depolarization during the action potential inactivates sodium channels, which then require tens to hundreds of milliseconds to become available for subsequent action potentials.…”